Abstract
The ectomycorrhizal symbiosis was long thought to be restricted to temperate forests. However, as tropical forests have been explored, it has become clear that these habitats host unique ectomycorrhizal (ECM) fungi. We have been exploring tropical dry forests (TDF), which are endangered terrestrial ecosystems and hotspots of endemism. Since Fabaceae is the main plant family in this environment, we hypothesized that trees in this lineage would be the main ECM hosts. We sequenced the ITS rDNA region from fungi and both rbcL and trnL cpDNA from plants to identify both symbiotic partners from root tips. The systematic position of each symbiont was confirmed by Bayesian phylogenetic inference. We identified 20 plant species belonging to 10 families that hosted 19 unique ECM fungal species from 5 lineages. Most ECM fungi were associated with Caryophyllales, not with Fabaceae. Achatocarpus and Guapira, the main hosts, are scattered throughout the forest and are not in monodominant patches. The low ECM fungal diversity can be explained by the low density of host plants and their high specificity. Our results indicate that Caryophyllales is an important order of tropical ECM hosts with at least four independent evolutionary lineages that have evolved the ability to form ectomycorrhizae.
Similar content being viewed by others
References
Agerer R, Rambold G (2004-2017) DEEMY—an information system for characterization and determination of ectomycorrhizae. München, Germany URL wwwdeemyde. Accessed 18 Mar 2017
Alexander I (2006) Ectomycorrhizas—out of Africa? New Phytol 172:589–591
Alvarez-Añorve MY, Quesada M, Sanchez-Azofeifa GA et al (2012) Functional regeneration and spectral reflectance of trees during succession in a highly diverse tropical dry forest ecosystem. Am J Bot 99:816–826. https://doi.org/10.3732/ajb.1100200
Alvarez-Manjarrez J, Villegas-Ríos M, Garibay-Orijel R et al (2016) Tomentella brunneoincrustata, the first described species of the Pisonieae-associated Neotropical Tomentella clade, and phylogenetic analysis of the genus in Mexico. Mycol Prog 15:1–11. https://doi.org/10.1007/s11557-015-1152-x
Anaya CA, García-Oliva F, Jaramillo VJ (2007) Rainfall and labile carbon availability control litter nitrogen dynamics in a tropical dry forest. Oecologia 150:602–610. https://doi.org/10.1007/s00442-006-0564-3
Ángeles-Argáiz RE, Flores-García A, Ulloa M, Garibay-Orijel R (2016) Commercial Sphagnum peat moss is a vector for exotic ectomycorrhizal mushrooms. Biol Invasions 18:89–101. https://doi.org/10.1007/s10530-015-0992-2
Argüelles-Moyao A, Garibay-Orijel R, Márquez-Valdelamar LM, Arellano-Torres E (2017) Clavulina-Membranomyces is the most important lineage within the highly diverse ectomycorrhizal fungal community of Abies religiosa. Mycorrhiza 27:53–67. https://doi.org/10.1007/s00572-016-0724-1
Ashford A, Allaway W (1982) A sheathing mycorrhiza on Pisonia grandis R. Br. (Nyctaginaceae) with development of transfer cells rather than a Hartig net. New Phytol 90:511–519. https://doi.org/10.1111/j.1469-8137.1982.tb04483.x
Bâ AM, Duponnois R, Moyersoen B, Diédhiou AG (2012) Ectomycorrhizal symbiosis of tropical African trees. Mycorrhiza 22:1–29. https://doi.org/10.1007/s00572-011-0415-x
Bahram M, Kõljalg U, Courty P-E et al (2013) The distance decay of similarity in communities of ectomycorrhizal fungi in different ecosystems and scales. J Ecol 101:1335–1344. https://doi.org/10.1111/1365-2745.12120
Bandala VM, Montoya L, Villegas R (2011) Tremelloscypha gelatinosa (Sebacinales) from tropical deciduous Gymnopodium forests in southern Mexico. Mycotaxon 118:147–157. https://doi.org/10.5248/118.147
Bandou E, Lebailly F, Muller F, Dulormne M (2006) The ectomycorrhizal fungus Scleroderma bermudense alleviates salt stress in seagrape (Coccoloba uvifera L.) seedlings. Mycorrhiza 16:559–565. https://doi.org/10.1007/s00572-006-0073-6
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77. https://doi.org/10.1007/s11104-008-9877-9
Bullock SH (1986) Climate of Chamela, Jalisco, and trends in the south coastal region of Mexico. Arch Meteor Geophy B 36:297–316. https://doi.org/10.1007/BF02263135
Burke JM, Sanchez A (2011) Revised subfamily classification for Polygonaceae, with a tribal classification for Eriogonoideae. Brittonia 63:510–520. https://doi.org/10.1007/s12228-011-9197-x
Campo J, Jaramillo VJ, Maass JM (1998) Pulses of soil phosphorus availability in a tropical dry forest: effects of seasonally and level of wetting. Oecologia 115:167–172. https://doi.org/10.1007/s004420050504
Campo J, Maass JM, Jaramillo VJ, Martínez Yrízar A (2000) Calcium, potassium, and magnesium cycling in a Mexican tropical dry forest ecosystem. Biogeochemistry 49:21–36. https://doi.org/10.1023/A:1006207319622
Chambers SM, Hitchcock CJ, Cairney JWG (2005) Ectomycorrhizal mycobionts of Pisonia grandis on coral cays in the Capricorn-bunker group, great barrier reef, Australia. Mycol Res 109:1105–1111. https://doi.org/10.1017/S0953756205003576
Corrales A, Arnold AE, Ferrer A et al (2016) Variation in ectomycorrhizal fungal communities associated with Oreomunnea mexicana (Juglandaceae) in a Neotropical montane forest. Mycorrhiza 26:1–17. https://doi.org/10.1007/s00572-015-0641-8
Crawley SS, Hilu KW (2012) Impact of missing data, gene choice, and taxon sampling on phylogenetic reconstruction: the Caryophyllales (angiosperms). Plant Syst Evol 298:297–312. https://doi.org/10.1007/s00606-011-0544-x
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772. https://doi.org/10.1038/nmeth.2109
Dell B, Sanmee R, Lumyong P, Lumyong S (2005) Ectomycorrhizal fungi in dry and wet dipterocarp forests in northern Thailand—diversity and use as food. Proceeding of the 8 th round-table conference on dipterocarps. Ho chi Minh City, Vietnam: 1–11
Dickie IA (2007) Host preference, niches and fungal diversity. New Phytol 174:230–233. https://doi.org/10.1111/j.1469-8137.2007.02055.x
Diédhiou AG, Selosse M-A, Galiana A et al (2010) Multi-host ectomycorrhizal fungi are predominant in a Guinean tropical rainforest and shared between canopy trees and seedlings. Environ Microbiol 12:2219–2232. https://doi.org/10.1111/j.1462-2920.2010.02183.x
DRYFLOR (2016) Plant diversity patterns of the Neotropical dry forest and their conservation implicatons. Science 353:1383–1387. https://doi.org/10.1126/science.aaf5080
Ducousso M, Ramanankierana H, Duponnois R et al (2008) Mycorrhizal status of native trees and shrubs from eastern Madagascar littoral forests with special emphasis on one new ectomycorrhizal endemic family, the Asteropeiaceae. New Phytol 178:233–238. https://doi.org/10.1111/j.1469-8137.2008.02389.x
Durán E, Balvanera P, Lott E et al (2002) Estructura, composición y dinámica de la vegetación. In: Noguera FA, Vega Rivera JH, García Aldrete AN, Quesada Avendaño M (eds) Historia Natural de Chamela. Instituto de Biología, UNAM, México
Ebenye HCM, Taudière A, Niang N et al (2016) Ectomycorrhizal fungi are shared between seedlings and adults in a monodominant Gilbertiodendron dewevrei rain forest in Cameroon. Biotropica:1–12. https://doi.org/10.1111/btp.12415
Fukami T, Nakajima M, Fortunel C et al (2017) Geographical variation in community divergence: insights from tropical forest monodominance by ectomycorrhizal trees. Am Nat 190:S105–S122. https://doi.org/10.1086/692439
García-Oliva F, Maass JM, Galicia L (1995) Rainstorm analysis and rainfall of a seasonal region with strong cyclonic influence on the Pacific Coast of Mexico. J Appl Meteorol 34:2491–2498. https://doi.org/10.1175/1520-0450(1995)034<2491:RAAREO>2.0.CO;2
Garibay Orijel R, Morales-Marañon E, Domínguez-Gutiérrez M, Flores-García A (2013) Caracterización morfológica y genética de las ectomicorrizas formadas entre Pinus montezumae y los hongos presentes en los bancos de esporas en la Faja Volcánica Transmexicana. Rev Mex Biodivers 84:153–169. https://doi.org/10.7550/rmb.29839
Gentry AH (1988) Changes in plant community diversity and floristic composition on environmental and geographical gradients. Ann Mo Bot Gard 75:1–34
Haug I, Weiss M, Homeier J et al (2005) Russulaceae and Thelephoraceae form ectomycorrhizas with members of the Nyctaginaceae (Caryophyllales) in the tropical mountain rain forest of southern Ecuador. New Phytol 165:923–936. https://doi.org/10.1111/j.1469-8137.2004.01284.x
Hayward JA, Horton TR (2012) Edaphic factors do not govern the ectomycorrhizal specificity of Pisonia grandis (Nyctaginaceae). Mycorrhiza 22:647–652. https://doi.org/10.1007/s00572-012-0442-2
van der Heijden MG, Martin FM, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423. https://doi.org/10.1111/nph.13288
Imhof S (2009) Arbuscular, ecto-related, orchid mycorrhizas—three independent structural lineages towards mycoheterotrophy: implications for classification? Mycorrhiza 19:357–363. https://doi.org/10.1007/s00572-009-0240-7
Ishida TA, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer-broadleaf forests. New Phytol 174:430–440. https://doi.org/10.1111/j.1469-8137.2007.02016.x
Janzen D (1988) Tropical dry forest. The most endangered major tropical ecosystems. In: Wilson EO (ed) Biodiversity. Nactional Academy Press, Washington, DC, pp 130–137
Kennedy PG, Matheny PB, Ryberg KM et al (2012) Scaling up: examining the macroecology of ectomycorrhizal fungi. Mol Ecol 21:4151–4154. https://doi.org/10.1111/j.1365-294X.2012.05703.x
Kornerup A, Wanscher JH (1978) Methuen handbook of colour, 3rd edn. Eyre Methuen, London
Kress WJ, Erickson DL (2007) A two-locus global DNA barcode for land plants: the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS One 2:e508. https://doi.org/10.1371/journal.pone.0000508
Linares-Palomino R, Oliveira-Filho AT, Pennington TR (2006) Neotropical seasonally dry forests: diversity, endemism, and biogeography of woody plants. In: Dirzo R, Young HS, Mooney HA, Ceballos G (eds) Seasonally dry tropical forests: ecology and conservation. Island Press, Washington, D.C.
Looney BP, Ryberg M, Hampe F et al (2016) Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi. Mol Ecol 25:630–647. https://doi.org/10.1111/mec.13506
Lott EJ (1993) Annotated checklist of the vascular flora of the Chamela Bay region. Occas Pap Calif Acad Sci 148:1–60
Lott EJ, Atkinson TH (2002) Biodiversidad y fitogeografía de Chamela-Cuixmala, Jalisco. In: Noguera FA, Vega Rivera JH, García Aldrete AN, Quesada Avendaño M (eds) Historia Natural de Chamela. Instituto de Biología, UNAM, México
Magallón S, Castillo A (2009) Angiosperm diversification through time. Am J Bot 96:349–365. https://doi.org/10.3732/ajb.0800060
Maherali H, Oberle B, Stevens PF et al (2016) Mutualism persistence and abandonment during the evolution of the mycorrhizal symbiosis. Am Nat 188:E113–E125. https://doi.org/10.1086/688675
Martínez-Yrízar A, Sarukhán J (1993) Cambios estacionales del mantillo en el suelo de un bosque tropical caducifolio y subcaducifolio en Chamela, Jalisco, México. Acta Bot Mex 21:1–6
Matheny PB, Aime MC, Bougher NL et al (2009) Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae. J Biogeogr 36:577–592. https://doi.org/10.1111/j.1365-2699.2008.02055.x
McGuire KL, Henkel TW, Granzow De La Cerda I et al (2008) Dual mycorrhizal colonization of forest-dominating tropical trees and the mycorrhizal status of non-dominant tree and liana species. Mycorrhiza 18:217–222. https://doi.org/10.1007/s00572-008-0170-9
Miles L, Newton AC, DeFries RS et al (2006) A global overview of the conservation status of tropical dry forests. J Biogeogr 33:491–505. https://doi.org/10.1111/j.1365-2699.2005.01424.x
Peay KG (2016) The mutualistic niche: mycorrhizal symbiosis and community dynamics. Annu Rev Ecol Evol Syst 47:143–164. https://doi.org/10.1146/annurev-ecolsys-121415-032100
Peay K, Kennedy P, Davies S et al (2010) Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol 185:529–542. https://doi.org/10.1111/j.1469-8137.2009.03075.x
Pendry CA (2004) Monograph of Ruprechtia (Polygonaceae). Syst Bot Monogr 67:1–113. https://doi.org/10.2307/25027911
Põlme S, Bahram M, Yamanaka T et al (2013) Biogeography of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale. New Phytol 198:1239–1249. https://doi.org/10.1111/nph.12170
Portillo-Quintero CA, Sánchez-Azofeifa GA (2010) Extent and conservation of tropical dry forests in the Americas. Biol Conserv 143:144–155. https://doi.org/10.1016/j.biocon.2009.09.020
Ramirez-Lopez I, Villegas-Rios M, Salas-Lizana R et al (2015) Thelephora versatilis and Thelephora pseudoversatilis: two new cryptic species with polymorphic basidiomes inhabiting tropical deciduous and sub-perennial forests of the Mexican Pacific coast. Mycologia 107:346–358. https://doi.org/10.3852/14-151
Ronquist F, Huelsenbeck JP (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Roy M, Schimann H, Braga-Neto R et al (2016) Diversity and distribution of ectomycorrhizal fungi in Amazonian lowland white sand forests. Biotropica 48:90–100. https://doi.org/10.1111/btp.12297
Rzedowski J (1991) El endemismo en la flora fanerogámica mexicana: una apreciación analítica preliminar. Acta Bot Mex 15:47–64
Sandoval-Zapotitla E (2005) Técnicas aplicadas al estudio de la anatomía vegetal. Cuadernos 38. Instituto de Biología, Universidad Nacional Autónoma México, México
Schäferhoff B, Müller KF, Borsch T (2009) Caryophyllales phylogenetics: disentangling Phytolaccaceae and Molluginaceae and description of Microteaceae as a new isolated family. Willdenowia 39:209–228. https://doi.org/10.3372/wi.39.39201
Séne S, Avril R, Chaintreuil C et al (2015) Ectomycorrhizal fungal communities of Coccoloba uvifera (L.) L. mature trees and seedlings in the neotropical coastal forests of Guadeloupe (Lesser Antilles). Mycorrhiza 25:547–559. https://doi.org/10.1007/s00572-015-0633-8
Singer R (1988) The role of fungi in periodically inundated Amazonian forests. Vegetatio 78:27–30. https://doi.org/10.1007/BF00045636
Smith ME, Douhan GW, Rizzo DM (2007) Intra-specific and intra-sporocarp ITS variation of ectomycorrhizal fungi as assessed by rDNA sequencing of sporocarps and pooled ectomycorrhizal roots from a Quercus woodland. Mycorrhiza 18:15–22. https://doi.org/10.1007/s00572-007-0148-z
Smith ME, Henkel TW, Catherine Aime M et al (2011) Ectomycorrhizal fungal diversity and community structure on three co-occurring leguminous canopy tree species in a Neotropical rainforest. New Phytol 192:699–712. https://doi.org/10.1111/j.1469-8137.2011.03844.x
Smith ME, Henkel TW, Williams GC et al (2017) Investigating niche partitioning of ectomycorrhizal fungi in specialized rooting zones of the monodominant leguminous tree Dicymbe corymbosa. New Phytol. https://doi.org/10.1111/nph.14570
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109. https://doi.org/10.1007/BF00037152
Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biol Rev 27:83–99. https://doi.org/10.1016/j.fbr.2013.09.001
Tedersoo L, Suvi T, Beaver K, Kõljalg U (2007) Ectomycorrhizal fungi of the Seychelles: diversity patterns and host shifts from the native Vateriopsis seychellarum (Dipterocarpaceae) and Intsia bijuga (Caesalpiniaceae) to the introduced Eucalyptus robusta (Myrtaceae), but not Pinus caribea (Pinaceae). New Phytol 175:321–333. https://doi.org/10.1111/j.1469-8137.2007.02104.x
Tedersoo L, Jairus T, Horton BM et al (2008) Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytol 180:479–490. https://doi.org/10.1111/j.1469-8137.2008.02561.x
Tedersoo L, Sadam A, Zambrano M et al (2010) Low diversity and high host preference of ectomycorrhizal fungi in western Amazonia, a neotropical biodiversity hotspot. ISME J 4:465–471. https://doi.org/10.1038/ismej.2009.131
Tedersoo L, Bahram M, Toots M et al (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 21:4160–4170. https://doi.org/10.1111/j.1365-294X.2012.05602.x
Tedersoo L, Bahram M, Ryberg M et al (2014a) Global biogeography of the ectomycorrhizal /sebacina lineage (fungi, Sebacinales) as revealed from comparative phylogenetic analyses. Mol Ecol 23:4168–4183. https://doi.org/10.1111/mec.12849
Tedersoo L, Bahram M, Polme S et al (2014b) Global diversity and geography of soil fungi. Science 346:6213. https://doi.org/10.1126/science.1256688
Trejo I, Dirzo R (2002) Floristic diversity of Mexican seasonally dry tropical forests. Biodivers Conserv 11:2063–2084. https://doi.org/10.1023/A:1020876316013
Wang B, Qiu Y-L (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363. https://doi.org/10.1007/s00572-005-0033-6
Waring BG, Adams R, Branco S, Powers JS (2016) Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests. New Phytol 209:845–854. https://doi.org/10.1111/nph.13654
Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214. https://doi.org/10.1089/10665270050081478
Acknowledgments
This study was funded by CONACYT Ciencia Básica 239266 and PAPIIT IN223114. The MEXBOL network supported DNA sequencing through the CONACYT 1251085 grant. We thank to Posgrado en Ciencias Biológicas from Universidad Nacional Autónoma de México. We acknowledge the Academic Writing Team of the Centro de Estudios de Posgrado, UNAM, for their help with this manuscript. MES received support from the US National Science Foundation grant DEB 1354802. We thank Leho Tedersoo and Jeremy Hayward for their assistance in the methodology for the plant identification. We are also thankful to Mohammad Bahram for his helpful comments, and two anonymous reviewers that improved the article. We thank Estela Sandoval-Zapotitla for her help at the anatomical slices of ectomycorrhizae. We thank to the Biological Station of Chamela and its entire staff.
Author information
Authors and Affiliations
Contributions
J.A.M. and R.G.O. were responsible for the experimental design. J.A.M. made the field work, laboratory proceedings, and the data analysis. J.A.M., R.G.O., and M.E.S. wrote the manuscript.
Corresponding author
Rights and permissions
About this article
Cite this article
Alvarez-Manjarrez, J., Garibay-Orijel, R. & Smith, M.E. Caryophyllales are the main hosts of a unique set of ectomycorrhizal fungi in a Neotropical dry forest. Mycorrhiza 28, 103–115 (2018). https://doi.org/10.1007/s00572-017-0807-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-017-0807-7